Rapid Bidirectional Reorganization of Cortical Microcircuits

Abstract

Mature neocortex adapts to altered sensory input by changing neural activity in cortical circuits. The underlying cellular mechanisms remain unclear. We used blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to show reorganization in somatosensory cortex elicited by altered whisker sensory input. We found that there was rapid expansion followed by retraction of whisker cortical maps. The cellular basis for the reorganization in primary somatosensory cortex was investigated with paired electrophysiological recordings in the periphery of the expanded whisker representation. During map expansion, the chance of finding a monosynaptic connection between pairs of pyramidal neurons increased 3-fold. Despite the rapid increase in local excitatory connectivity, the average strength and synaptic dynamics did not change, which suggests that new excitatory connections rapidly acquire the properties of established excitatory connections. During map retraction, entire excitatory connections between pyramidal neurons were lost. In contrast, connectivity between pyramidal neurons and fast spiking interneurons was unchanged. Hence, the changes in local excitatory connectivity did not occur in all circuits involving pyramidal neurons. Our data show that pyramidal neurons are recruited to and eliminated from local excitatory networks over days. These findings suggest that the local excitatory connectome is dynamic in mature neocortex.

Reorganization of Recurrent Layer 5 Corticospinal Networks Following Adult Motor Training

“…Although our examination was confined to layer 5 corticospinal neurons of the motor cortex, theoretical and computational models suggest that targeted reorganization of recurrent networks is likely to be a general property of cortex. Indeed, whiskertrimming paradigms in rodents have shown reorganization of recurrent synaptic circuitry in barrel cortex (Cheetham et al, 2007;Albieri et al, 2015). The extent of which these results further generalize across different cell types and brain regions should be the focus of future experimental inquiry.…”

Size-Dependent Axonal Bouton Dynamics following Visual Deprivation In Vivo

“…Sensory experience modifies synaptic strength and connectivity between cortical neurons ( Cheetham et al., 2007 , Albieri et al., 2015 ). Theoretical studies suggest that the distribution of synaptic strengths both processes sensory input and provides a substrate to encode experience ( Barbour et al., 2007 , Stepanyants and Escobar, 2011 ).…”

“…Diminished sensory experience can induce synapse loss but its effect on surviving synapses is less clear ( Barnes et al., 2015a , Barnes et al., 2017 ). Conditions that drive synapse loss may weaken surviving synapses ( Albieri et al., 2015 , Barnes et al., 2015a ) or trigger homeostatic changes in strength ( Barnes et al., 2017 ). Alternately, prolonged loss of sensory activity may shape the distribution of surviving synaptic strengths.…”

Perceptually relevant remapping of human somatotopy in 24 hours

“…A comparable process of reduced inhibition prior to remapping has been reported in studies of sensory deprivation in rodent barrel cortex. Reduced inputs after whisker clipping produce a local pattern of cortical disinhibition and broadening excitation, followed by subsequent cortical contraction of the representation (Albieri et al, 2015). In this case, changes in the relative inputs across different digits may prompt a transient disinhibitory cortical milieu, and the subsequent re-establishment of modified excitatory networks within the cortex, wherein the cortical representations have shifted to reflect new usage patterns.…”